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Impact of Fermentable Protein, by Feeding High Protein Diets, on Microbial Composition, Microbial Catabolic Activity, Gut Health and Beyond in Pigs

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Impact of Fermentable Protein, by Feeding High Protein Diets, on Microbial Composition, Microbial Catabolic Activity, Gut Health and Beyond in Pigs microorganisms Review Impact of Fermentable Protein, by Feeding High Protein Diets, on Microbial Composition, Microbial Catabolic Activity, Gut Health and beyond in Pigs Hanlu Zhang 1,2, Nikkie van der Wielen 1,3, Bart van der Hee 4,5 , Junjun Wang 2 , Wouter Hendriks 1 and Myrthe Gilbert 1,* 1 Animal Nutrition Group, Department of Animal Sciences, Wageningen University, 338, 6700 AH Wageningen, The Netherlands; [email protected] (H.Z.); [email protected] (N.v.d.W.); [email protected] (W.H.) 2 State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China; [email protected] 3 Division of Human Nutrition and Health, Department of Agrotechnology and Food Sciences, Wageningen University, Stippenengm 4, 6708 WE Wageningen, The Netherlands 4 Host-Microbe Interactomics Group, Department of Animal Sciences, Wageningen University, 338, 6700 AH Wageningen, The Netherlands; [email protected] 5 Laboratory of Microbiology, Department of Agrotechnology and Food Sciences, Wageningen University, Stippeneng 4, 6708 WE Wageningen, The Netherlands * Correspondence: [email protected] Received: 30 September 2020; Accepted: 4 November 2020; Published: 5 November 2020 Abstract: In pigs, high protein diets have been related to post-weaning diarrhoea, which may be due to the production of protein fermentation metabolites that were shown to have harmful effects on the intestinal epithelium in vitro. In this review, we discussed in vivo effects of protein fermentation on the microbial composition and their protein catabolic activity as well as gut and overall health. The reviewed studies applied different dietary protein levels, which was assumed to result in contrasting fermentable protein levels. A general shift to N-utilisation microbial community including potential pathogens was observed, although microbial richness and diversity were not altered in the majority of the studies. Increasing dietary protein levels resulted in higher protein catabolic activity as evidenced by increased concentration of several protein fermentation metabolites like biogenic amines in the digesta of pigs. Moreover, changes in intestinal morphology, permeability and pro-inflammatory cytokine concentrations were observed and diarrhoea incidence was increased. Nevertheless, higher body weight and average daily gain were observed upon increasing dietary protein level. In conclusion, increasing dietary protein resulted in higher proteolytic fermentation, altered microbial community and intestinal physiology. Supplementing diets with fermentable carbohydrates could be a promising strategy to counteract these effects and should be further investigated. Keywords: protein fermentation; dietary protein; microbial composition; fermentation metabolites; gut health; pig 1. Introduction Proteins, peptides and amino acids (AA) in the gastrointestinal tract of pigs, either from exogenous or endogenous origin, can be utilised by the inhabitant microbiota. This utilisation first requires the breakdown of larger proteins and peptides by microbiota-derived proteases and peptidases, so-called proteolytic activity [1]. Subsequently, AA and short peptides act as building blocks for microbial protein synthesis or they can be utilised as an energy source, often referred to as protein fermentation [2]. Microorganisms 2020, 8, 1735; doi:10.3390/microorganisms8111735 www.mdpi.com/journal/microorganisms Microorganisms 2020, 8, 1735 2 of 23 This dissimilatory metabolism is less energetically favourable compared to carbohydrate catabolism [3] and leads to a series of metabolites of which several have the potential to negatively affect the gut in vitro [4]. Protein fermentation is thought to occur mostly in the large intestine because of its greater microbial population and slower passage rate compared to the small intestine [5]. Dietary proteins, as well as endogenous proteinaceous material such as digestive enzymes, sloughed epithelial cells, mucins and microbes [6], reach the large intestine when not digested and absorbed in the upper gastrointestinal tract. Approximately 15 to 25% of the dietary proteins in a conventional pig diet reach the large intestine [7], but this can be greatly influenced by the dietary protein level and the digestibility of the included protein source [8,9]. Moreover, the fate of these proteins in the large intestine depends on the quantity and type of dietary fermentable carbohydrates present [10]. High protein diets have been related to decreased faecal consistency and increased incidence of post-weaning diarrhoea in pigs [11,12], with protein fermentation processes suspected as being the underlying cause [4]. The current review focuses on the effects of protein fermentation in vivo by comparing microbial composition, the formation of metabolites and gut health between pigs fed with increased dietary protein levels compared to pigs fed with lower protein levels. 2. Changes in Microbial Composition The intestinal microbiota plays a major role in the modulation of host physiology and metabolism, including nutrient utilisation, bioavailability, energy status and immune system development [13,14]. After birth, the intestinal tract is rapidly colonised by microbiota and its composition changes over time in response to diet, stress and disease state [15,16]. Diet is a large driver of microbial composition in the intestine, especially at a young age, as bacterial composition is still developing and is neither stable nor resilient; microbiota composition in adult pigs is assumed to be relatively stable [17,18]. As such, weaning piglets are expected to be more prone to microbial changes in response to diet, with increased indigestible protein potentially related to unfavourable health outcomes. Multiple studies have investigated the effects of dietary protein on microbial composition and host health [19–21]. However, there are several factors that make comparisons between such studies rather difficult. For example, the methodology used to analyse and report microbial composition varies, e.g., utilising different reference databases for operational taxonomic units (OTU) clustering, different sequencing techniques or genomic regions or depth of analysis. For instance, culture-based studies were only able to identify a few groups of known bacteria that were preselected by researchers. In the majority of these studies, total Coliforms and E. coli are chosen to represent potential harmful species and Lactobacilli are chosen to represent beneficial species [22–24]. Although culture-independent DNA sequencing methods have been developed [25], studies are still limited due to the required probes and incompleteness of the databases to analyse sequenced data. As not all microbes can be identified by OTU clustering methods due to similarity in sequenced gene regions, results on microbial composition and classification should be compared cautiously. Furthermore, sequencing of various regions of the hypervariable region sequencing (V) of the 16S SSU rRNA gene also affects the estimated results, where the V3/V4 region has shown the highest classification accuracy [26], but more recent studies signify the importance of utilising long-read sequencing of the full 16S gene to overcome inter- and intragenomic variation to more accurately estimate community profiles [27]. In addition, most studies calculate relative abundance from sequenced composition, but it is likely that microbial composition and biological implications are different when expressed in absolute abundance, rather than in relative abundance [28]. Other factors that may lead to differences in microbial composition results between studies [12,19,22] may be related to physiology such as intestinal segment and age or variation in other dietary components, especially fermentable carbohydrate. The microbial composition is known to vary between intestinal segments and factors such as pH and substrate availability in these segments play a role [29]. When increasing protein level, changes in microbial composition also showed segment-dependent changes across the jejunum, caecum, colon and in faeces. For instance, Microorganisms 2020, 8, 1735 3 of 23 the proportions of major phyla were altered by protein level only in the ileum, but not in the colon [30]. In addition, the ileal microbiota structure can show different responses to an increase in dietary protein compared to the colon, especially at the family and genus level [31]. Despite the limitations for comparing studies, effects of dietary protein level on general trends in microbial composition can be summarised and are discussed below. Microbial richness and diversity are important parameters in host–microbe symbiosis. Upon increasing crude protein level in the diet, the microbial richness and diversity, i.e., number and variety of OTUs, was found unaltered in most studies (Table1). Nevertheless, some studies showed a temporary increase in microbial richness and diversity when providing higher dietary protein levels to pigs [31–34]. The richer and more diverse colonic microbiota of weanling piglets reported was possibly related to the enterotoxigenic Escherichia coli challenge and was only observed seven days post-challenge, although no effect on total Coliforms was observed in these piglets [32]. In general, higher microbiota richness and diversity is considered beneficial and protective [35,36]. However, this was not related to an advantageous health outcome and even worse faecal score was observed [32],
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